1,812
Views
61
CrossRef citations to date
0
Altmetric
Original Research Articles

Extracellular vesicles, tissue factor, cancer and thrombosis – discussion themes of the ISEV 2014 Educational Day

, , , , , , , , , , , , , , & show all
Article: 26901 | Received 12 Jul 2014, Accepted 18 Feb 2015, Published online: 13 Mar 2015

References

  • Bouillaud S, Bouillaud J. De l'Obliteration des veines et de son influence sur la formation des hydropisies partielles: consideration sur la hydropisies passive et general. Archiv Gen Med. 1823; 1: 188–204.
  • Buller HR, van Doormaal FF, van Sluis GL, Kamphuisen PW. Cancer and thrombosis: from molecular mechanisms to clinical presentations. J Thromb Haemost. 2007; 5: 246–54.
  • Geddings JE, Mackman N. Tumor-derived tissue factor-positive microparticles and venous thrombosis in cancer patients. Blood. 2013; 122: 1873–80.
  • Dvorak HF, Van DeWater L, Bitzer AM, Dvorak AM, Anderson D, Harvey VS et al. Procoagulant activity associated with plasma membrane vesicles shed by cultured tumour cells. Cancer Res. 1983; 43: 4434–42. [PubMed Abstract].
  • Bastida E, Ordinas A, Escolar G, Jamieson GA. Tissue factor in microvesicles shed from U87MG human glioblastoma cells induces coagulation, platelet aggregation, and thrombogenesis. Blood. 1984; 64: 177–84. [PubMed Abstract].
  • Davila M, Amirkhosravi A, Coll E, Desai H, Robles L, Colon J et al. Tissue factor-bearing microparticles derived from tumour cells: impact on coagulation activation. J Thromb Haemost. 2008; 6: 1517–24.
  • Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011; 144: 646–74.
  • Heppner GH. Tumor cell societies. J Natl Cancer Inst. 1989; 81: 648–9.
  • Wu M, Pastor-Pareja JC, Xu T. Interaction between Ras(V12) and scribbled clones induces tumour growth and invasion. Nature. 2010; 463: 545–8.
  • Suva ML, Rheinbay E, Gillespie SM, Patel AP, Wakimoto H, Rabkin SD et al. Reconstructing and reprogramming the tumour-propagating potential of glioblastoma stem-like cells. Cell. 2014; 157: 580–94.
  • Rak J. Extracellular vesicles - biomarkers and effectors of the cellular interactome in cancer. Front Pharmacol. 2013; 4: 21.
  • Al-Nedawi K, Meehan B, Micallef J, Lhotak V, May L, Guha A et al. Intercellular transfer of the oncogenic receptor EGFRvIII by microvesicles derived from tumour cells. Nat Cell Biol. 2008; 10: 619–24.
  • Skog J, Wurdinger T, van RS, Meijer DH, Gainche L, Sena-Esteves M et al. Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol. 2008; 10: 1470–6.
  • Balaj L, Lessard R, Dai L, Cho YJ, Pomeroy SL, Breakefield XO et al. Tumour microvesicles contain retrotransposon elements and amplified oncogene sequences. Nat Commun. 2011; 2: 180.
  • Lee TH, Chennakrishnaiah S, Audemard E, Montermini L, Meehan B, Rak J. Oncogenic ras-driven cancer cell vesiculation leads to emission of double-stranded DNA capable of interacting with target cells. Biochem Biophys Res Commun. 2014; 451: 295–301.
  • Yu X, Harris SL, Levine AJ. The regulation of exosome secretion: a novel function of the p53 protein. Cancer Res. 2006; 66: 4795–801.
  • Putz U, Howitt J, Doan A, Goh CP, Low LH, Silke J et al. The tumour suppressor PTEN is exported in exosomes and has phosphatase activity in recipient cells. Sci Signal. 2012; 5: ra70.
  • Gabriel K, Ingram A, Austin R, Kapoor A, Tang D, Majeed F et al. Regulation of the tumour suppressor PTEN through exosomes: a diagnostic potential for prostate cancer. PLoS One. 2013; 8: e70047.
  • Valadi H, Ekstrom K, Bossios A, Sjostrand M, Lee JJ, Lotvall JO. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol. 2007; 9: 654–9.
  • Quesenberry PJ, Goldberg LR, Aliotta JM, Dooner MS, Pereira MG, Wen S et al. Cellular phenotype and extracellular vesicles: basic and clinical considerations. Stem Cells Dev. 2014; 23: 1429–36.
  • Wolf P. The nature and significance of platelet products in human plasma. Br J Haematol. 1967; 13: 269–88.
  • Taylor DD, Doellgast GJ. Quantitation of peroxidase-antibody binding to membrane fragments using column chromatography. Anal Biochem. 1979; 98: 53–9.
  • Poste G, Nicolson GL. Arrest and metastasis of blood-borne tumour cells are modified by fusion of plasma membrane vesicles from highly metastatic cells. Proc Natl Acad Sci USA. 1980; 77: 399–403.
  • Johnstone RM. Exosomes biological significance: a concise review. Blood cells Mol Dis. 2006; 36: 315–21.
  • Thery C, Ostrowski M, Segura E. Membrane vesicles as conveyors of immune responses. Nat Rev Immunol. 2009; 9: 581–93.
  • Bobrie A, Thery C. Exosomes and communication between tumours and the immune system: are all exosomes equal?. Biochem Soc Trans. 2013; 41: 263–7.
  • Shen B, Wu N, Yang JM, Gould SJ. Protein targeting to exosomes/microvesicles by plasma membrane anchors. J Biol Chem. 2011; 286: 14383–95.
  • Bolukbasi MF, Mizrak A, Ozdener GB, Madlener S, Strobel T, Erkan EP et al. miR-1289 and “Zipcode”-like Sequence Enrich mRNAs in Microvesicles. Mol Ther Nucleic Acids. 2012; 1: e10.
  • Gibbings DJ, Ciaudo C, Erhardt M, Voinnet O. Multivesicular bodies associate with components of miRNA effector complexes and modulate miRNA activity. Nat Cell Biol. 2009; 11: 1143–9.
  • Zwicker JI, Trenor CC 3rd, Furie BC, Furie B. Tissue factor-bearing microparticles and thrombus formation. Arterioscler Thromb Vasc Biol. 2011; 31: 728–33.
  • Nieuwland R. Cellular origin of microparticles exposing tissue factor in cancer: a mixed double?. J Thromb Haemost. 2008; 6: 1514–16. [PubMed Abstract].
  • Peinado H, Aleckovic M, Lavotshkin S, Matei I, Costa-Silva B, Moreno-Bueno G et al. Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET. Nat Med. 2012; 18: 883–91.
  • Janowska-Wieczorek A, Marquez-Curtis LA, Wysoczynski M, Ratajczak MZ. Enhancing effect of platelet-derived microvesicles on the invasive potential of breast cancer cells. Transfusion. 2006; 46: 1199–209.
  • El-Andaloussi S, Lee Y, Lakhal-Littleton S, Li J, Seow Y, Gardiner C et al. Exosome-mediated delivery of siRNA in vitro and in vivo. Nat Protoc. 2012; 7: 2112–26.
  • Mignot G, Roux S, Thery C, Segura E, Zitvogel L. Prospects for exosomes in immunotherapy of cancer. J Cell Mol Med. 2006; 10: 376–88.
  • Al-Nedawi K, Meehan B, Rak J. Microvesicles: messengers and mediators of tumour progression. Cell Cycle. 2009; 8: 2014–18.
  • Garnier D, Jabado N, Rak J. Extracellular vesicles as prospective carriers of oncogenic protein signatures in adult and paediatric brain tumours. Proteomics. 2013; 13: 1595–607.
  • Chen WW, Balaj L, Liau LM, Samuels ML, Kotsopoulos SK, Maguire CA et al. BEAMing and droplet digital PCR analysis of mutant IDH1 mRNA in glioma patient serum and cerebrospinal fluid extracellular vesicles. Mol Ther Nucleic Acids. 2013; 2: e109.
  • Noerholm M, Balaj L, Limperg T, Salehi A, Zhu LD, Hochberg FH et al. RNA expression patterns in serum microvesicles from patients with glioblastoma multiforme and controls. BMC Cancer. 2012; 12: 22.
  • Shao H, Chung J, Balaj L, Charest A, Bigner DD, Carter BS et al. Protein typing of circulating microvesicles allows real-time monitoring of glioblastoma therapy. Nat Med. 2012; 18: 1835–40.
  • Bergsmedh A, Szeles A, Henriksson M, Bratt A, Folkman MJ, Spetz AL et al. Horizontal transfer of oncogenes by uptake of apoptotic bodies. Proc Natl Acad Sci USA. 2001; 98: 6407–11.
  • Kahlert C, Melo SA, Protopopov A, Tang J, Seth S, Koch M et al. Identification of double-stranded genomic DNA spanning all chromosomes with mutated KRAS and p53 DNA in the serum exosomes of patients with pancreatic cancer. J Biol Chem. 2014; 289: 3869–75.
  • Thakur BK, Zhang H, Becker A, Matei I, Huang Y, Costa-Silva B et al. Double-stranded DNA in exosomes: a novel biomarker in cancer detection. Cell Res. 2014; 24: 766–9.
  • Garcia-Olmo DC, Dominguez C, Garcia-Arranz M, Anker P, Stroun M, Garcia-Verdugo JM et al. Cell-free nucleic acids circulating in the plasma of colorectal cancer patients induce the oncogenic transformation of susceptible cultured cells. Cancer Res. 2010; 70: 560–7.
  • Al-Nedawi K, Meehan B, Kerbel RS, Allison AC, Rak J. Endothelial expression of autocrine VEGF upon the uptake of tumour-derived microvesicles containing oncogenic EGFR. Proc Natl Acad Sci USA. 2009; 106: 3794–9.
  • Demory Beckler M, Higginbotham JN, Franklin JL, Ham AJ, Halvey PJ, Imasuen IE et al. Proteomic analysis of exosomes from mutant KRAS colon cancer cells identifies intercellular transfer of mutant KRAS. Mol Cell Proteomics. 2013; 12: 343–55.
  • Luga V, Zhang L, Viloria-Petit AM, Ogunjimi AA, Inanlou MR, Chiu E et al. Exosomes mediate stromal mobilization of autocrine Wnt-PCP signaling in breast cancer cell migration. Cell. 2012; 151: 1542–56.
  • Antonyak MA, Li B, Boroughs LK, Johnson JL, Druso JE, Bryant KL et al. Cancer cell-derived microvesicles induce transformation by transferring tissue transglutaminase and fibronectin to recipient cells. Proc Natl Acad Sci USA. 2011; 108: 4852–7.
  • Di Vizio D, Kim J, Hager MH, Morello M, Yang W, Lafargue CJ et al. Oncosome formation in prostate cancer: association with a region of frequent chromosomal deletion in metastatic disease. Cancer Res. 2009; 69: 5601–9.
  • Koumangoye RB, Sakwe AM, Goodwin JS, Patel T, Ochieng J. Detachment of breast tumour cells induces rapid secretion of exosomes which subsequently mediate cellular adhesion and spreading. PLoS One. 2011; 6: e24234.
  • Tauro BJ, Mathias RA, Greening DW, Gopal SK, Ji H, Kapp EA et al. Oncogenic H-ras reprograms Madin-Darby canine kidney (MDCK) cell-derived exosomal proteins following epithelial-mesenchymal transition. Mol Cell Proteomics. 2013; 12: 2148–59.
  • Garnier D, Magnus N, Lee TH, Bentley V, Meehan B, Milsom C et al. Cancer cells induced to express mesenchymal phenotype release exosome-like extracellular vesicles carrying tissue factor. J Biol Chem. 2012; 287: 43565–72.
  • Garnier D, Magnus N, Meehan B, Kislinger T, Rak J. Qualitative changes in the proteome of extracellular vesicles accompanying cancer cell transition to mesenchymal state. Exp Cell Res. 2013; 319: 2747–57.
  • Gesierich S, Berezovskiy I, Ryschich E, Zoller M. Systemic induction of the angiogenesis switch by the tetraspanin D6.1A/CO-029. Cancer Res. 2006; 66: 7083–94.
  • Svensson KJ, Kucharzewska P, Christianson HC, Skold S, Lofstedt T, Johansson MC et al. Hypoxia triggers a proangiogenic pathway involving cancer cell microvesicles and PAR-2-mediated heparin-binding EGF signaling in endothelial cells. Proc Natl Acad Sci USA. 2011; 108: 13147–52.
  • Kucharzewska P, Christianson HC, Welch JE, Svensson KJ, Fredlund E, Ringner M et al. Exosomes reflect the hypoxic status of glioma cells and mediate hypoxia-dependent activation of vascular cells during tumour development. Proc Natal Acad Sci USA. 2013; 110: 7312–17.
  • Bussolati B, Grange C, Camussi G. Tumor exploits alternative strategies to achieve vascularization. FASEB J. 2011; 25: 2874–82.
  • Janowska-Wieczorek A, Wysoczynski M, Kijowski J, Marquez-Curtis L, Machalinski B, Ratajczak J et al. Microvesicles derived from activated platelets induce metastasis and angiogenesis in lung cancer. Int J Cancer. 2005; 113: 752–60.
  • Thaler J, Preusser M, Ay C, Kaider A, Marosi C, Zielinski C et al. Intratumoral tissue factor expression and risk of venous thromboembolism in brain tumour patients. Thromb Res. 2013; 131: 162–5.
  • Sartori MT, Della Puppa A, Ballin A, Campello E, Radu CM, Saggiorato G et al. Circulating microparticles of glial origin and tissue factor bearing in high-grade glioma: a potential prothrombotic role. Thromb Haemost. 2013; 110: 378–85.
  • Milsom CC, Yu JL, Mackman N, Micallef J, Anderson GM, Guha A et al. Tissue factor regulation by epidermal growth factor receptor and epithelial-to-mesenchymal transitions: effect on tumour initiation and angiogenesis. Cancer Res. 2008; 68: 10068–76.
  • Yu JL, May L, Lhotak V, Shahrzad S, Shirasawa S, Weitz JI et al. Oncogenic events regulate tissue factor expression in colorectal cancer cells: implications for tumour progression and angiogenesis. Blood. 2005; 105: 1734–41.
  • Clark SR, Thomas CP, Hammond VJ, Aldrovandi M, Wilkinson GW, Hart KW et al. Characterization of platelet aminophospholipid externalization reveals fatty acids as molecular determinants that regulate coagulationm. Proc Natl Acad Sci USA. 2013; 110: 5875–80.
  • Mackman N. The many faces of tissue factor. J Thromb Haemost. 2009; 7: 136–9.
  • van den Berg YW, Osanto S, Reitsma PH, Versteeg HH. The relationship between tissue factor and cancer progression: insights from bench and bedside. Blood. 2012; 119: 924–32.
  • Mackman N, Luther T. Platelet tissue factor: to be or not to be. Thromb Res. 2013; 132: 3–5.
  • Wang JG, Geddings JE, Aleman MM, Cardenas JC, Chantrathammachart P, Williams JC et al. Tumor-derived tissue factor activates coagulation and enhances thrombosis in a mouse xenograft model of human pancreatic cancer. Blood. 2012; 119: 5543–52.
  • Thomas GM, Panicot-Dubois L, Lacroix R, Dignat-George F, Lombardo D, Dubois C. Cancer cell-derived microparticles bearing P-selectin glycoprotein ligand 1 accelerate thrombus formation in vivo. J Exp Med. 2009; 206: 1913–27.
  • Hron G, Kollars M, Weber H, Sagaster V, Quehenberger P, Eichinger S et al. Tissue factor-positive microparticles: cellular origin and association with coagulation activation in patients with colorectal cancer. Thromb Haemost. 2007; 97: 119–23. [PubMed Abstract].
  • Haubold K, Rink M, Spath B, Friedrich M, Chun FK, Marx G et al. Tissue factor procoagulant activity of plasma microparticles is increased in patients with early-stage prostate cancer. Thromb Haemost. 2009; 101: 1147–55. [PubMed Abstract].
  • Tesselaar ME, Romijn FP, van der Linden IK, Prins FA, Bertina RM, Osanto S. Microparticle-associated tissue factor activity: a link between cancer and thrombosis?. J Thromb Haemost. 2007; 5: 520–7.
  • Manly DA, Wang J, Glover SL, Kasthuri R, Liebman HA, Key NS et al. Increased microparticle tissue factor activity in cancer patients with Venous Thromboembolism. Thromb Res. 2010; 125: 511–12.
  • Tesselaar ME, Romijn FP, van der Linden IK, Bertina RM, Osanto S. Microparticle-associated tissue factor activity in cancer patients with and without thrombosis. J Thromb Haemost. 2009; 7: 1421–3.
  • Zwicker JI, Liebman HA, Neuberg D, Lacroix R, Bauer KA, Furie BC et al. Tumor-derived tissue factor-bearing microparticles are associated with venous thromboembolic events in malignancy. Clin Cancer Res. 2009; 15: 6830–40.
  • Campello E, Spiezia L, Radu CM, Bulato C, Castelli M, Gavasso S et al. Endothelial, platelet, and tissue factor-bearing microparticles in cancer patients with and without venous thromboembolism. Thromb Res. 2011; 127: 473–7.
  • Thaler J, Ay C, Mackman N, Bertina RM, Kaider A, Marosi C et al. Microparticle-associated tissue factor activity, venous thromboembolism and mortality in pancreatic, gastric, colorectal and brain cancer patients. J Thromb Haemost. 2012; 10: 1363–70.
  • Bharthuar A, Khorana AA, Hutson A, Wang JG, Key NS, Mackman N et al. Circulating microparticle tissue factor, thromboembolism and survival in pancreaticobiliary cancers. Thromb Res. 2013; 132: 180–4.
  • van Es N, Bleker S, Kleinjan A, Berckmans RJ, Wilmink JW, Nieuwland R et al. A new microparticle coagulant activity assay to predict venous thromboembolism in patients with pancreatic cancer. The American Society of Hematology. 2014 Dec 4–9; San Francisco, CA Abstract 4250.
  • Zwicker JI, Liebman HA, Bauer KA, Caughey T, Campigotto F, Rosovsky R et al. Prediction and prevention of thromboembolic events with enoxaparin in cancer patients with elevated tissue factor-bearing microparticles: a randomized-controlled phase II trial (the Microtec study). Br J Haematol. 2013; 160: 530–7.
  • Aalberts M, van Dissel-Emiliani FM, van Adrichem NP, van WM, Wauben MH, Stout TA et al. Identification of distinct populations of prostasomes that differentially express prostate stem cell antigen, annexin A1, and GLIPR2 in humans. Biol Reprod. 2012; 86: 82.
  • Khorana AA, Streiff MB, Farge D, Mandala M, Debourdeau P, Cajfinger F et al. Venous thromboembolism prophylaxis and treatment in cancer: a consensus statement of major guidelines panels and call to action. J Clin Oncol. 2009; 27: 4919–26.
  • Mukherjee SD, Swystun LL, Mackman N, Wang JG, Pond G, Levine MN et al. Impact of chemotherapy on thrombin generation and on the protein C pathway in breast cancer patients. Pathophysiol Haemost Thromb. 2010; 37: 88–97.
  • Collier ME, Ettelaie C. Regulation of the incorporation of tissue factor into microparticles by serine phosphorylation of the cytoplasmic domain of tissue factor. J Biol Chem. 2011; 286: 11977–84.
  • Dorfleutner A, Ruf W. Regulation of tissue factor cytoplasmic domain phosphorylation by palmitoylation. Blood. 2003; 102: 3998–4005.
  • Zioncheck TF, Roy S, Vehar GA. The cytoplasmic domain of tissue factor is phosphorylated by a protein kinase C-dependent mechanism. J Biol Chem. 1992; 267: 3561–4. [PubMed Abstract].
  • Ott I, Fischer EG, Miyagi Y, Mueller BM, Ruf W. A role for tissue factor in cell adhesion and migration mediated by interaction with actin-binding protein 280. J Cell Biol. 1998; 140: 1241–53.
  • Collier ME, Maraveyas A, Ettelaie C. Filamin-A is required for the incorporation of tissue factor into cell-derived microvesicles. Thromb Haemost. 2014; 111: 647–55.
  • Ettelaie C, Elkeeb AM, Maraveyas A, Collier ME. p38alpha phosphorylates serine 258 within the cytoplasmic domain of tissue factor and prevents its incorporation into cell-derived microparticles. Biochim Biophys Acta. 2013; 1833: 613–21.
  • Vion AC, Birukova AA, Boulanger CM, Birukov KG. Mechanical forces stimulate endothelial microparticle generation via caspase-dependent apoptosis-independent mechanism. Pulm Circ. 2013; 3: 95–9.
  • Camerer E, Gjernes E, Wiiger M, Pringle S, Prydz H. Binding of factor VIIa to tissue factor on keratinocytes induces gene expression. J Biol Chem. 2000; 275: 6580–5.
  • Belting M, Dorrell MI, Sandgren S, Aguilar E, Ahamed J, Dorfleutner A et al. Regulation of angiogenesis by tissue factor cytoplasmic domain signaling. Nat Med. 2004; 10: 502–9.
  • Collier ME, Ettelaie C. Induction of endothelial cell proliferation by recombinant and microparticle-tissue factor involves beta1-integrin and extracellular signal regulated kinase activation. Arterioscler Thromb Vasc Biol. 2010; 30: 1810–17.
  • Kocaturk B, Van den Berg YW, Tieken C, Mieog JS, de Kruijf EM, Engels CC et al. Alternatively spliced tissue factor promotes breast cancer growth in a beta1 integrin-dependent manner. Proc Natl Acad Sci USA. 2013; 110: 11517–22.
  • Pradier A, Ettelaie C. The influence of exogenous tissue factor on the regulators of proliferation and apoptosis in endothelial cells. J Vasc Res. 2008; 45: 19–32.
  • Frentzou GA, Collier ME, Seymour AM, Ettelaie C. Differential induction of cellular proliferation, hypertrophy and apoptosis in H9c2 cardiomyocytes by exogenous tissue factor. Mol Cell Biochem. 2010; 345: 119–30.
  • Aharon A, Tamari T, Brenner B. Monocyte-derived microparticles and exosomes induce procoagulant and apoptotic effects on endothelial cells. Thromb Haemost. 2008; 100: 878–85. [PubMed Abstract].
  • Collier ME, Mah PM, Xiao Y, Maraveyas A, Ettelaie C. Microparticle-associated tissue factor is recycled by endothelial cells resulting in enhanced surface tissue factor activity. Thromb Haemost. 2013; 110: 966–76.
  • Liou YC, Zhou XZ, Lu KP. Prolyl isomerase Pin1 as a molecular switch to determine the fate of phosphoproteins. Trends Biochem Scie. 2011; 36: 501–14.
  • Bach RR, Moldow CF. Mechanism of tissue factor activation on HL-60 cells. Blood. 1997; 89: 3270–6. [PubMed Abstract].
  • Wolberg AS, Monroe DM, Roberts HR, Hoffman MR. Tissue factor de-encryption: ionophore treatment induces changes in tissue factor activity by phosphatidylserine-dependent and -independent mechanisms. Blood Coagul Fibrinolysis. 1999; 10: 201–10.
  • Chen VM, Ahamed J, Versteeg HH, Berndt MC, Ruf W, Hogg PJ. Evidence for activation of tissue factor by an allosteric disulfide bond. Biochemistry. 2006; 45: 12020–8.
  • Mandal SK, Iakhiaev A, Pendurthi UR, Rao LV. Acute cholesterol depletion impairs functional expression of tissue factor in fibroblasts: modulation of tissue factor activity by membrane cholesterol. Blood. 2005; 105: 153–60.
  • Mandal SK, Pendurthi UR, Rao LV. Cellular localization and trafficking of tissue factor. Blood. 2006; 107: 4746–53.
  • Dietzen DJ, Page KL, Tetzloff TA. Lipid rafts are necessary for tonic inhibition of cellular tissue factor procoagulant activity. Blood. 2004; 103: 3038–44.
  • Sevinsky JR, Rao LV, Ruf W. Ligand-induced protease receptor translocation into caveolae: a mechanism for regulating cell surface proteolysis of the tissue factor-dependent coagulation pathway. J Cell Biol. 1996; 133: 293–304.
  • Berckmans RJ, Sturk A, van Tienen LM, Schaap MC, Nieuwland R. Cell-derived vesicles exposing coagulant tissue factor in saliva. Blood. 2011; 117: 3172–80.
  • van Doormaal F, Kleinjan A, Berckmans RJ, Mackman N, Manly D, Kamphuisen PW et al. Coagulation activation and microparticle-associated coagulant activity in cancer patients. An exploratory prospective study. Thromb Haemost. 2012; 108: 160–5.
  • Milsom C, Yu J, May L, Magnus N, Rak J. Diverse roles of tissue factor-expressing cell subsets in tumour progression. Semin Thromb Hemost. 2008; 34: 170–81.
  • Bailey KM, Wojtkowiak JW, Hashim AI, Gillies RJ. Targeting the metabolic microenvironment of tumors. Adv Pharmacol. 2012; 65: 63–107. [PubMed Abstract] [PubMed CentralFull Text].
  • Kucharzewska P, Belting M. Emerging roles of extracellular vesicles in the adaptive response of tumour cells to microenvironmental stress. J Extracell Vesicles. 2013; 2: 20304. http://dx.doi.org/10.3402/jev.v2i0.20304.
  • van der Pol E, Boing AN, Harrison P, Sturk A, Nieuwland R. Classification, functions, and clinical relevance of extracellular vesicles. Pharmacol Rev. 2012; 64: 676–705.
  • van der Pol E, Coumans F, Varga Z, Krumrey M, Nieuwland R. Innovation in detection of microparticles and exosomes. J Thromb Haemost. 2013; 11: 36–45.
  • van der Pol E, van Gemert MJ, Sturk A, Nieuwland R, van Leeuwen TG. Single vs. swarm detection of microparticles and exosomes by flow cytometry. J Thromb Haemost. 2012; 10: 919–30.
  • van der Vlist EJ, Nolte-‘t Hoen EN, Stoorvogel W, Arkesteijn GJ, Wauben MH. Fluorescent labeling of nano-sized vesicles released by cells and subsequent quantitative and qualitative analysis by high-resolution flow cytometry. Nat Protoc. 2012; 7: 1311–26.
  • van der Pol E, Coumans FA, Grootemaat AE, Gardiner C, Sargent IL, Harrison P et al. Particle size distribution of exosomes and microvesicles determined by transmission electron microscopy, flow cytometry, nanoparticle tracking analysis, and resistive pulse sensing. J Thromb Haemost. 2014; 12: 1182–92.
  • Gardiner C, Ferreira YJ, Dragovic RA, Redman CW, Sargent IL. Extracellular vesicle sizing and enumeration by nanoparticle tracking analysis. J Extracell Vesicles. 2013; 2 http://dx.doi.org/10.3402/jev.v2i0.19671.
  • Arraud N, Linares R, Tan S, Gounou C, Pasquet JM, Mornet S et al. Extracellular vesicles from blood plasma: determination of their morphology, size, phenotype and concentration. J Thromb Haemost. 2014; 12: 614–27.
  • Tatsumi K, Antoniak S, Monroe DM 3rd, Khorana AA, Mackman N. Evaluation of a new commercial assay to measure microparticle tissue factor activity in plasma: communication from the SSC of the ISTH. J Thromb Haemost. 2014; 12: 1932–4.
  • Basavaraj MG, Olsen JO, Osterud B, Hansen JB. Differential ability of tissue factor antibody clones on detection of tissue factor in blood cells and microparticles. Thromb Res. 2012; 130: 538–46.
  • Verhaak RG, Hoadley KA, Purdom E, Wang V, Qi Y, Wilkerson MD et al. Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1. Cancer Cell. 2010; 17: 98–110.
  • Ay C, Dunkler D, Marosi C, Chiriac AL, Vormittag R, Simanek R et al. Prediction of venous thromboembolism in cancer patients. Blood. 2010; 116: 5377–82.
  • Perry JR. Thromboembolic disease in patients with high-grade glioma. Neuro Oncol. 2012; 14: iv73–80.
  • Blom JW, Vanderschoot JP, Oostindier MJ, Osanto S, van der Meer FJ, Rosendaal FR. Incidence of venous thrombosis in a large cohort of 66,329 cancer patients: results of a record linkage study. J Thromb Haemost. 2006; 4: 529–35.
  • Spyropoulos AC, Lin J. Direct medical costs of venous thromboembolism and subsequent hospital readmission rates: an administrative claims analysis from 30 managed care organizations. J Manag Care Pharm. 2007; 13: 475–86. [PubMed Abstract].
  • Brandes AA, Scelzi E, Salmistraro G, Ermani M, Carollo C, Berti F et al. Incidence of risk of thromboembolism during treatment high-grade gliomas: a prospective study. Eur J Cancer. 1997; 33: 1592–6.
  • Magnus N, Gerges N, Jabado N, Rak J. Coagulation-related gene expression profile in glioblastoma is defined by molecular disease subtype. J Thromb Haemost. 2013; 11: 1197–200.
  • Magnus N, Garnier D, Rak J. Oncogenic epidermal growth factor receptor up-regulates multiple elements of the tissue factor signaling pathway in human glioma cells. Blood. 2010; 116: 815–18.
  • Perry JR, Julian JA, Laperriere NJ, Geerts W, Agnelli G, Rogers LR et al. PRODIGE: a randomized placebo-controlled trial of dalteparin low-molecular-weight heparin thromboprophylaxis in patients with newly diagnosed malignant glioma. J Thromb Haemost. 2010; 8: 1959–65.
  • Gonda DD, Akers JC, Kim R, Kalkanis SN, Hochberg FH, Chen CC et al. Neuro-oncologic applications of exosomes, microvesicles, and other nano-sized extracellular particles. Neurosurgery. 2013; 72: 501–10.